HomeSearch by dateVacation packagesHotelsFlight dealsCar rentalTravel tips & news
St. John's

$299+ Cheap flights from Colorado to St. John's (ANU)

This is the cheapest one-way flight price found by a Cheapflights user in the last 72 hours by searching for a flight departing on 12/13. Fares are subject to change and may not be available on all flights or dates of travel.
DEN — ANU
Dec 6 — Dec 131
Sat 12/6
Sat 12/13
1 adult, Economy
We work with more than 300 partners to bring you better travel deals

Find cheap flights from Colorado to St. John's with Cheapflights

1. Tell us where you want to go

Enter your travel information like dates, passengers, trip type (one-way or round trip), and preferred cabin class then click “Find deals”

2. Select your favorite providers

We find the providers serving your travel needs. Choose up to four travel providers to compare side-by-side for flights, hotels, or car rentals.

3. Compare prices and book

Review each provider’s pricing and select the best option for you! Book through your favorite provider’s website for a seamless experience.

Find flight deals from Colorado to St. John's

Cheapest flights from Colorado to St. John's
Explore the most affordable flight options available from Colorado to St. John's. Find the lowest fares from popular airlines and budget airlines, with prices last updated on November 6, 2025.

This Priceline deal was found by Cheapflights users on 11/6. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure Priceline is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Sat 12/611:50 amDEN - ANU
1 stop24h 03mJetBlue
Sat 12/133:59 pmANU - DEN
1 stop22h 06mJetBlue
Deal found 11/6$601
This American Airlines deal was found by Cheapflights users on 11/6. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Fri 12/122:23 pmDRO - ANU
2 stops19h 57mAmerican Airlines
Fri 12/192:49 pmANU - DRO
2 stops21h 58mAmerican Airlines
Deal found 11/6$604
This Priceline deal was found by Cheapflights users on 11/6. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure Priceline is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Fri 12/511:21 pmDEN - ANU
1 stop12h 51mJetBlue
Fri 12/124:18 pmANU - DEN
1 stop32h 49mJetBlue
Deal found 11/6$671
This American Airlines deal was found by Cheapflights users on 11/5. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Thu 12/1111:59 pmDEN - ANU
1 stop11h 12mAmerican Airlines
Sat 12/204:04 pmANU - DEN
1 stop10h 55mAmerican Airlines
Deal found 11/5$699
This American Airlines deal was found by Cheapflights users on 11/6. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Fri 12/54:42 pmDEN - ANU
2 stops21h 16mAmerican Airlines
Fri 12/126:03 pmANU - DEN
2 stops22h 50mAmerican Airlines
Deal found 11/6$704
This American Airlines deal was found by Cheapflights users on 11/6. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Thu 12/411:59 pmDEN - ANU
1 stop11h 12mAmerican Airlines
Wed 12/103:30 pmANU - DEN
1 stop10h 33mAmerican Airlines
Deal found 11/6$730
This American Airlines deal was found by Cheapflights users on 11/5. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Tue 11/2512:17 amDEN - ANU
1 stop13h 29mAmerican Airlines
Wed 12/33:30 pmANU - DEN
1 stop10h 33mAmerican Airlines
Deal found 11/5$794
This American Airlines deal was found by Cheapflights users on 11/6. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Sat 12/64:42 pmDEN - ANU
2 stops21h 16mAmerican Airlines
Sat 12/133:28 pmANU - DEN
2 stops23h 03mAmerican Airlines
Deal found 11/6$876
This Mytrip deal was found by Cheapflights users on 11/4. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure Mytrip is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Wed 12/31:25 pmDEN - ANU
1 stop22h 55mMultiple Airlines
Wed 12/104:20 pmANU - DEN
2 stops28h 24mMultiple Airlines
Deal found 11/4$1,017
This Delta deal was found by Cheapflights users on 11/6. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure Delta is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Fri 12/512:50 amDEN - ANU
1 stop10h 55mDelta
Sat 12/134:00 pmANU - DEN
1 stop9h 53mDelta
Deal found 11/6$1,019
This American Airlines deal was found by Cheapflights users on 11/4. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Sat 11/158:25 amDRO - ANU
2 stops25h 50mAmerican Airlines
Wed 11/195:47 pmANU - DRO
2 stops31h 08mAmerican Airlines
Deal found 11/4$1,060
This American Airlines deal was found by Cheapflights users on 11/5. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Sun 11/97:00 amMTJ - ANU
2 stops27h 15mAmerican Airlines
Thu 11/135:47 pmANU - MTJ
2 stops28h 32mAmerican Airlines
Deal found 11/5$1,209

Cheap flight deals from Colorado to St. John's

Keep the following information in mind while searching for Colorado to St. John's flight deals. Data was last updated November 6, 2025.

Most accurate provider

eDreams
3 stars

Most trusted provider

eDreams
3 stars

Round-trip from

$563
(Expedia)

One-way from

$299
(American Airlines)

Popular in

December

Cheapest in

February

Average price

$844
Provider with most accurate pricing for Denver Intl-St. John's V.C. Bird Intl flight deals.
Search Deals
Provider most trusted by Cheapflights users for Denver Intl-St. John's V.C. Bird Intl flights.
Search Deals
From Colorado to St. John's V.C. Bird Intl
Search Deals
One-way flight from Colorado to St. John's V.C. Bird Intl
Search Deals
Highest demand for flights based on searches. 4% potential increase in price ($42 potential increase over avg. RT price).
Search Deals
Cheapest flight prices on average. 2% potential price decrease ($22 potential savings vs. average RT price).
Search Deals
Average for round-trip flights in November 2025
Search Deals

Cheapflights Fare Finder

 
Customize your flight search to find flights from Colorado to St. John's that fit within your specific budget. Explore options based on user searches and filter the results based on your desired price range. Find flights that match your budget for a cost-effective journey. Over the last 7 days, Cheapflights users made 2,558,603 searches. Data last updated November 6, 2025.
Use the filters below to find and compare flights from Colorado to St. John's that are best for you.

Fly from

Colorado

Fly to

St. John's

Route

Depart

Return

Price

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Thu 3/5

11:59 pm-2:39 pm

1 stop11h 40m

St. John's V.C. Bird Intl

Thu 3/12

2:15 pm-8:45 am

1 stop20h 30m

$563

DurangoSt. John's

DRO - ANU

DROANU

Durango La Plata County

Fri 12/12

2:23 pm-1:20 pm

2 stops19h 57m

St. John's V.C. Bird Intl

Fri 12/19

2:49 pm-11:16 am

2 stops23h 27m

$604

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Fri 12/5

11:21 pm-3:12 pm

1 stop12h 51m

St. John's V.C. Bird Intl

Fri 12/12

4:18 pm-10:07 pm

1 stop32h 49m

$671

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Thu 12/11

11:59 pm-2:11 pm

1 stop11h 12m

St. John's V.C. Bird Intl

Sat 12/20

4:04 pm-11:59 pm

1 stop10h 55m

$699

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Sun 3/29

11:59 pm-1:20 pm

2 stops11h 21m

St. John's V.C. Bird Intl

Tue 4/7

3:50 pm-11:15 am

2 stops21h 25m

$704

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Tue 5/5

6:52 pm-3:25 pm

2 stops18h 33m

St. John's V.C. Bird Intl

Tue 5/12

2:20 pm-10:01 pm

1 stop9h 41m

$704

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Wed 4/8

1:00 am-3:25 pm

1 stop12h 25m

St. John's V.C. Bird Intl

Sat 4/18

3:50 pm-11:15 am

2 stops21h 25m

$704

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Fri 12/5

11:59 pm-2:12 pm

1 stop11h 13m

St. John's V.C. Bird Intl

Fri 12/12

6:03 pm-1:53 pm

2 stops22h 50m

$704

Grand JunctionSt. John's

GJT - ANU

GJTANU

Grand Junction Regnl

Sun 4/26

7:07 pm-12:14 pm

2 stops15h 07m

St. John's V.C. Bird Intl

Thu 4/30

3:50 pm-11:28 am

2 stops21h 38m

$714

DurangoSt. John's

DRO - ANU

DROANU

Durango La Plata County

Sat 12/13

2:23 pm-1:20 pm

2 stops19h 57m

$299

Flights are sorted by cheapest round-trip flights first.

Deals found on 11/5

Showing 1-10 of 14 results
1
2

Best time to book a flight from Colorado to St. John's

Have a flexible travel schedule? Discover the best time to fly to St. John's from Colorado with our price prediction graph.
Estimated round-trip price
Rates are based on past data. Find the cheapest month and day to book your flight based on your travel requirements, then search for cheap deals.

Cheapflights Insights

Everything you need to know about your flight from Colorado to St. John's

What is the cheapest month to book a flight from Colorado to St. John's, Saint John?

Currently, February is the cheapest month in which you can book a flight from Colorado to St. John's, Saint John (average of $374). Flying from Colorado to St. John's, Saint John in December is currently the most expensive (average of $749). There are several factors that can impact the price of a flight, so comparing airlines, departure airports and flight times can provide users with more options.

What is the cheapest time of day to fly from CO to ANU?

Find hourly flight availability from Colorado to St. John's. Discover flight options and departure times throughout the day, allowing you to choose a departure time that suits your schedule. Data last updated November 6, 2025.

A simple way to save on the total cost of your ticket is to fly from Colorado to St. John's, Saint John in the afternoon. If you’re flexible enough to do this you can expect to save up to 23% on your trip compared to booking a flight in the evening.

Related info for your journey

Find useful and relevant information for your journey from Colorado to St. John's. Access travel guides, tips, and recommendations to enhance your travel experience. Get information about local attractions, weather, transportation options, and more.

  • What airport do you fly into for flights to St. John's from Colorado?

    If you book a flight to St. John's from Colorado, you will be flying to V.C. Bird Intl, which is the city’s only airport. St. John's V.C. Bird Intl (ANU) is located 3.8 mi from the center of St. John's.

  • How long is the flight from Colorado to St. John's, Saint John?

    A quick flight from Colorado to St. John's, Saint John can take about 11h 40m. JetBlue provides one of the quickest options available for as low as $563. The distance from Colorado to St. John's, Saint John is about 2998 mi. This flight may include one or multiple stops.

  • What are the most popular routes from Colorado to St. John's, Saint John?

    The most popular flight routes from Colorado to St. John's, Saint John are Denver Intl - St. John's V.C. Bird Intl, Durango La Plata County - St. John's V.C. Bird Intl and Montrose County - St. John's V.C. Bird Intl.

  • Can I find deals for flights from Colorado to St. John's that include hotel bookings?

    Yes. In addition to deals on Colorado to St. John's flights, Cheapflights offers vacation packages that include both flights and hotel.

  • How can I find direct flights from Colorado to St. John's?

    After entering your origin and destination, apply the non-stop filter on the search result page to find direct flights from Colorado to St. John's.

  • Can I find deals for business class flights from Colorado to St. John's?

    Yes. Cheapflights offers flight deals from Colorado to St. John's by cabin class. In addition to browsing deals, you can also filter by cabin class on the search results page after making a search.

  • What is the cheapest month to book a flight from Colorado to St. John's, Saint John?

    Currently, February is the cheapest month in which you can book a flight from Colorado to St. John's, Saint John (average of $374). Flying from Colorado to St. John's, Saint John in December is currently the most expensive (average of $749). There are several factors that can impact the price of a flight, so comparing airlines, departure airports and flight times can provide users with more options.

See more FAQs

Browse thousands of different options on Cheapflights for your next trip

Toggle through the tabs below to find thousands of options on Cheapflights for your next trip.

Alternative routes for Colorado to St. John's

See prices for flight routes from nearby airports that may be better suited for you.
John F Kennedy Intl to St. John's flights
LaGuardia to St. John's flights
Newark to St. John's flights
Miami to St. John's flights
Boston to St. John's flights
O'Hare Intl to St. John's flights
Dulles Intl to St. John's flights
Baltimore to St. John's flights
Reagan-National to St. John's flights
Dallas/Fort Worth to St. John's flights
Raleigh to St. John's flights
Atlanta to St. John's flights
Detroit to St. John's flights
Charlotte to St. John's flights
Philadelphia to St. John's flights
Orlando to St. John's flights
Rochester to St. John's flights
Providence to St. John's flights
Minneapolis to St. John's flights
Los Angeles to St. John's flights
Buffalo to St. John's flights
Cleveland to St. John's flights
Seattle to St. John's flights
Fort Lauderdale to St. John's flights
Richmond to St. John's flights
Hartford to St. John's flights
Cincinnati to St. John's flights
Tampa to St. John's flights
Indianapolis to St. John's flights
New Orleans to St. John's flights
Denver to St. John's flights
San Francisco to St. John's flights
St. Louis to St. John's flights
Columbus to St. John's flights
Austin to St. John's flights
Charleston to St. John's flights
White Plains to St. John's flights
Fayetteville to St. John's flights
Nashville to St. John's flights
Kansas City to St. John's flights
Omaha to St. John's flights
San Diego to St. John's flights
Midway to St. John's flights
West Palm Beach to St. John's flights
Hobby to St. John's flights
George Bush Intcntl to St. John's flights
Milwaukee to St. John's flights
Pittsburgh to St. John's flights
Portland to St. John's flights
Gainesville to St. John's flights

Top 2 airlines flying from Colorado to St. John's

Discover the top 2 airlines that operate flights from Colorado to St. John's. Compare their services, reliability, and customer satisfaction ratings to choose the airline that best suits your travel preferences and needs. Over the last 7 days, Cheapflights users made 2,558,603 searches. Data last updated November 6, 2025.
AirlineCheapestAverageFlexibilityOn-time
JetBlueCheapest$563Average$679FlexibilityNo cancel feeOn-time62%
American AirlinesCheapest$698Average$805FlexibilityNo cancel feeOn-time71%

100% Free

Cheapflights is completely free to use, so you can start saving the moment you arrive.

Book with Flexibility

Our users can plan ahead with confidence and find flights with no change fees

Travel Smart

Millions of people come to us for their flight needs every year. We help make travel planning easy by providing useful insights and data-driven graphs that can inform your decisions.